Endothelial cell amplification of regulatory t cells is differentially modified by immunosuppressors and intravenous immunoglobulin

Frontiers in Immunology

Volumn 8, Issue DEC, 2017, Pages

  Lion, Julien ^a   Burbach, Maren ^a   Cross, Amy ^a   Poussin, Karine ^a   Taflin, Cécile ^a   Kaveri, Srini ^b   Haziot, Alain ^a   Glotz, Denis ^a,c,d   Mooney, Nuala ^a,c,d  

^a SAINT LOUIS HOSPITAL   (France)

^b INSERM   (France)

^c Epidemiology and Biostatistics Unit   (France)

^d LabEx Transplantex   (France)

Author keywords

CD54; Cyclosporine A; Endothelium; HLA; Interleukin 6; Mycophenolic acid; Organ transplantation; Th17

Indexed keywords

CYCLOSPORIN A; HLA DR ANTIGEN; IMMUNOGLOBULIN; IMMUNOSUPPRESSIVE AGENT; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 17; INTERLEUKIN 6; MESSENGER RNA; MYCOPHENOLIC ACID;

APOPTOSIS; ARTICLE; CELL EXPANSION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE RELEASE; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HMEC-1 CELL LINE; HUMAN; HUMAN CELL; IMMUNOREGULATION; INFLAMMATION; LEUKOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; RNA ISOLATION; T LYMPHOCYTE SUBPOPULATION;

EID: 85037995527     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.01761     Document Type: Article

References (55)

1. Halloran PF. Immunosuppressive drugs for kidney transplantation. N Engl J Med (2004) 351(26):2715-29. doi:10.1056/NEJMra033540
2. Crabtree GR. Generic signals and specific outcomes. Cell (1999) 96(5):611-4. doi:10.1016/S0092-8674(00)80571-1
3. Matsuda S, Shibasaki F, Takehana K, Mori H, Nishida E, Koyasu S. Two distinct action mechanisms of immunophilin-ligand complexes for the blockade of T-cell activation. EMBO Rep (2000) 1(5):428-34. doi:10.1093/embo-reports/kvd090
4. Lamas S. Cellular mechanisms of vascular injury mediated by calcineurin inhibitors. Kidney Int (2005) 68(2):898-907. doi:10.1111/j.1523-1755.2005.00472.x
5. Navarro-Antolín J, López-Muñoz MJ, Klatt P, Soria J, Michel T, Lamas S. Formation of peroxynitrite in vascular endothelial cells exposed to cyclosporine A. FASEB J (2001) 15(7):1291-3. doi:10.1096/fj.00-0636fje
6. Navarro-Antolín J, Redondo-Horcajo M, Zaragoza C, Alvarez-Barrientos A, Fernández AP, León-Gómez E, et al. Role of peroxynitrite in endothelial damage mediated by cyclosporine A. Free Radic Biol Med (2007) 42(3):394-403. doi:10.1016/j.freeradbiomed.2006.11.008
7. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A (1990) 87(4):1620-4. doi:10.1073/pnas.87.4.1620
8. Allison AC, Eugui EM. Mycophenolate mofetil and its mechanisms of action. Immunopharmacology (2000) 47(2-3):85-118. doi:10.1016/S0162-3109(00)00188-0
9. Heinschink A, Raab M, Daxecker H, Griesmacher A, Müller MM. In vitro effects of mycophenolic acid on cell cycle and activation of human lymphocytes. Clin Chim Acta (2000) 300(1):23-8. doi:10.1016/S0009-8981(00)00297-7
10. Wadia PP, Herrera ND, Abecassis MM, Tambur AR. Mycophenolic acid inhibits maturation and function of human dendritic cells and B cells. Hum Immunol (2009) 70(9):692-700. doi:10.1016/j.humimm.2009.05.002
11. Ephrem A, Misra N, Hassan G, Dasgupta S, Delignat S, Duong Van Huyen JP, et al. Immunomodulation of autoimmune and inflammatory diseases with intravenous immunoglobulin. Clin Exp Med (2005) 5(4):135-40. doi:10.1007/s10238-005-0079-y
12. Gold R, Stangel M, Dalakas MC. Drug Insight: the use of intravenous immunoglobulin in neurology[mdash]therapeutic considerations and practical issues. Nat Clin Pract Neurol (2007) 3(1):36-44. doi:10.1038/ncpneuro0376
13. Perez EE, Orange JS, Bonilla F, Chinen J, Chinn IK, Dorsey M, et al. Update on the use of immunoglobulin in human disease: a review of evidence. J Allergy ClinImmunol (2017) 139(3):S1-46. doi:10.1016/j.jaci.2016.09.023
14. Glotz D, Antoine C, Julia P, Suberbielle-Boissel C, Boudjeltia S, Fraoui R, et al. Desensitization and subsequent kidney transplantation of patients using intravenous immunoglobulins (IVIg). Am J Transplant (2002) 2(8):758-60. doi:10.1034/j.1600-6143.2002.20809.x
15. Jordan SC, Tyan D, Stablein D, McIntosh M, Rose S, Vo A, et al. Evaluation of intravenous immunoglobulin as an agent to lower allosensitization and improve transplantation in highly sensitized adult patients with end-stage renal disease: report of the NIH IG02 trial. J Am Soc Nephrol (2004) 15(12):3256-62. doi:10.1097/01.ASN.0000145878.92906.9F
16. Montgomery RA, Zachary AA, Racusen LC, Leffell MS, King KE, Burdick J, et al. Plasmapheresis and intravenous immune globulin provides effective rescue therapy for refractory humoral rejection and allows kidneys to be successfully transplanted into cross-match-positive recipients. Transplantation (2000) 70(6):887-95. doi:10.1097/00007890-200009270-00006
17. Samuelsson A, Towers TL, Ravetch JV. Anti-inflammatory activity of IVIG mediated through the inhibitory Fc receptor. Science (2001) 291(5503):484-6. doi:10.1126/science.291.5503.484
18. Bruhns P, Samuelsson A, Pollard JW, Ravetch JV. Colony-stimulating factor-1-dependent macrophages are responsible for IVIG protection in antibody-induced autoimmune disease. Immunity (2003) 18(4):573-81. doi:10.1016/S1074-7613(03)00080-3
19. Maddur MS, Vani J, Hegde P, Lacroix-Desmazes S, Kaveri SV, Bayry J. Inhibition of differentiation, amplification, and function of human TH17 cells by intravenous immunoglobulin. J Allergy ClinImmunol (2011) 127(3): 823-30.e1-7. doi:10.1016/j.jaci.2010.12.1102
20. Jin J, Gong J, Lin B, Li Y, He Q. FcγRIIb expression on B cells is associated with treatment efficacy for acute rejection after kidney transplantation. Mol Immunol (2017) 85:283-92. doi:10.1016/j.molimm.2017.03.006
21. Bayry J, Lacroix-Desmazes S, Carbonneil C, Misra N, Donkova V, Pashov A, et al. Inhibition of maturation and function of dendritic cells by intravenous immunoglobulin. Blood (2003) 101(2):758-65. doi:10.1182/blood-2002-05-1447
22. Trinath J, Hegde P, Sharma M, Maddur MS, Rabin M, Vallat JM, et al. Intravenous immunoglobulin expands regulatory T cells via induction of cyclooxygenase-2-dependent prostaglandin E2 in human dendritic cells. Blood (2013) 122(8):1419-27. doi:10.1182/blood-2012-11-468264
23. Tanaka J, Kitashoji A, Fukunaga Y, Kashihara J, Nakano A, Kamizono A. Intravenous immunoglobulin suppresses abortion relates to an increase in the CD44bright NK subset in recurrent pregnancy loss model mice1. Biol Reprod (2016) 95(2):1-10. doi:10.1095/biolreprod.116.138438
24. Kessel A, Ammuri H, Peri R, Pavlotzky ER, Blank M, Shoenfeld Y, et al. Intravenous immunoglobulin therapy affects T regulatory cells by increasing their suppressive function. J Immunol (2007) 179(8):5571-5. doi:10.4049/jimmunol.179.8.5571
25. Tha-In T, Metselaar HJ, Bushell AR, Kwekkeboom J, Wood KJ. Intravenous immunoglobulins promote skin allograft acceptance by triggering functional activation of CD4+Foxp3+ T cells. Transplantation (2010) 89(12):1446-55. doi:10.1097/TP.0b013e3181dd6bf1
26. Massoud AH, Guay J, Shalaby KH, Bjur E, Ablona A, Chan D, et al. Intravenous immunoglobulin attenuates airway inflammation through induction of forkhead box protein 3-positive regulatory T cells. J Allergy ClinImmunol (2012) 129(6): 1656-65.e3. doi:10.1016/j.jaci.2012.02.050
27. Massoud AH, Kaufman GN, Xue D, Béland M, Dembele M, Piccirillo CA, et al. Peripherally generated Foxp3+ regulatory T cells mediate the immunomodulatory effects of IVIg in allergic airways disease. J Immunol (2017) 198(7):2760-71. doi:10.4049/jimmunol.1502361
28. Cosio FG, Gloor JM, Sethi S, Stegall MD. Transplant glomerulopathy. Am J Transplant (2008) 8(3):492-6. doi:10.1111/j.1600-6143.2007.02104.x
29. Einecke G, Sis B, Reeve J, Mengel M, Campbell PM, Hidalgo LG, et al. Antibody-mediated microcirculation injury is the major cause of late kidney transplant failure. Am J Transplant (2009) 9(11):2520-31. doi:10.1111/j.1600-6143.2009.02799.x
30. Muczynski KA, Cotner T, Anderson SK. Unusual expression of human lymphocyte antigen class II in normal renal microvascular endothelium. Kidney Int (2001) 59(2):488-97. doi:10.1046/j.1523-1755.2001.059002488.x
31. Muczynski KA, Ekle DM, Coder DM, Anderson SK. Normal human kidney HLA-DR-expressing renal microvascular endothelial cells: characterization, isolation, and regulation of MHC class II expression. J Am Soc Nephrol (2003) 14(5):1336-48. doi:10.1097/01.ASN.0000061778.08085.9F
32. Manes TD, Shiao SL, Dengler TJ, Pober JS. TCR signaling antagonizes rapid IP-10-mediated transendothelial migration of effector memory CD4+ T cells. J Immunol (2007) 178(5):3237-43. doi:10.4049/jimmunol.178.5.3237
33. Lee Y-R, Yang IH, Lee YH, Im SA, Song S, Li H, et al. Cyclosporin A and tacrolimus, but not rapamycin, inhibit MHC-restricted antigen presentation pathways in dendritic cells. Blood (2005) 105(10):3951-5. doi:10.1182/blood-2004-10-3927
34. Imai A, Sahara H, Tamura Y, Jimbow K, Saito T, Ezoe K, et al. Inhibition of endogenous MHC class II-restricted antigen presentation by tacrolimus (FK506) via FKBP51. Eur J Immunol (2007) 37(7):1730-8. doi:10.1002/eji.200636392
35. Taflin C, Favier B, Baudhuin J, Savenay A, Hemon P, Bensussan A, et al. Human endothelial cells generate Th17 and regulatory T cells under inflammatory conditions. Proc Natl Acad Sci U S A (2011) 108(7):2891-6. doi:10.1073/pnas.1011811108
36. Bestard O, Cruzado JM, Rama I, Torras J, Gomà M, Serón D, et al. Presence of FoxP3+ regulatory T cells predicts outcome of subclinical rejection of renal allografts. J Am Soc Nephrol (2008) 19(10):2020-6. doi:10.1681/ASN.2007111174
37. Deteix C, Attuil-Audenis V, Duthey A, Patey N, McGregor B, Dubois V, et al. Intragraft Th17 infiltrate promotes lymphoid neogenesis and hastens clinical chronic rejection. J Immunol (2010) 184(9):5344-51. doi:10.4049/jimmunol.0902999
38. Krustrup D, Madsen CB, Iversen M, Engelholm L, Ryder LP, Andersen CB. The number of regulatory T cells in transbronchial lung allograft biopsies is related to FoxP3 mRNA levels in bronchoalveolar lavage fluid and to the degree of acute cellular rejection. Transpl Immunol (2013) 29(1):71-5. doi:10.1016/j.trim.2013.08.002
39. Krystufkova E, Sekerkova A, Striz I, Brabcova I, Girmanova E, Viklicky O. Regulatory T cells in kidney transplant recipients: the effect of induction immunosuppression therapy. Nephrol Dial Transplant (2012) 27(6):2576-82. doi:10.1093/ndt/gfr693
40. Louis S, Braudeau C, Giral M, Dupont A, Moizant F, Robillard N, et al. Contrasting CD25hiCD4+T Cells/FOXP3 patterns in chronic rejection and operational drug-free tolerance. Transplantation (2006) 81(3):398-407. doi:10.1097/01.tp.0000203166.44968.86
41. Tang Q, Vincenti F. Transplant trials with Tregs: perils and promises. J Clin Invest (2017) 127(7):2505-12. doi:10.1172/JCI90598
42. Lion J, Taflin C, Cross AR, Robledo-Sarmiento M, Mariotto E, Savenay A, et al. HLA class II antibody activation of endothelial cells promotes Th17 and disrupts regulatory T lymphocyte expansion. Am J Transplant (2016) 16(5):1408-20. doi:10.1111/ajt.13644
43. Hauser IA, Johnson DR, Thévenod F, Goppelt-Strübe M. Effect of mycophenolic acid on TNFα-induced expression of cell adhesion molecules in human venous endothelial cells in vitro. Br J Pharmacol (1997) 122(7):1315-22. doi:10.1038/sj.bjp.0701517
44. Raab M, Daxecker H, Karimi A, Markovic S, Cichna M, Markl P, et al. In vitro effects of mycophenolic acid on the nucleotide pool and on the expression of adhesion molecules of human umbilical vein endothelial cells. Clin Chim Acta (2001) 310(1):89-98. doi:10.1016/S0009-8981(01)00527-7
45. Olejarz W, Bryk D, Zapolska-Downar D, Malecki M, Stachurska A, Sitkiewicz D. Mycophenolic acid attenuates the tumour necrosis factor-a-mediated proinflammatory response in endothelial cells by blocking the MAPK/NF-κB and ROS pathways. Eur J Clin Invest (2014) 44(1):54-64. doi:10.1111/eci.12191
46. Kolls JK, Lindén A. Interleukin-17 family members and inflammation. Immunity (2004) 21(4):467-76. doi:10.1016/j.immuni.2004.08.018
47. Jane-wit D, Manes TD, Yi T, Qin L, Clark P, Kirkiles-Smith NC, et al. Alloantibody and complement promote T cell-mediated cardiac allograft vasculopathy through noncanonical nuclear factor-κB signaling in endothelial cells. Circulation (2013) 128(23):2504-16. doi:10.1161/CIRCULATIONAHA.113.002972
48. Fu H, Kishore M, Gittens B, Wang G, Coe D, Komarowska I, et al. Self-recognition of the endothelium enables regulatory T-cell trafficking and defines the kinetics of immune regulation. Nat Commun (2014) 5:3436. doi:10.1038/ncomms4436
49. Krupnick AS, Gelman AE, Barchet W, Richardson S, Kreisel FH, Turka LA, et al. Cutting edge: murine vascular endothelium activates and induces the generation of allogeneic CD4+25+Foxp3+ regulatory T cells. J Immunol (2005) 175(10):6265-70. doi:10.4049/jimmunol.175.10.6265
50. Lemaître PH, Vokaer B, Charbonnier LM, Iwakura Y, Field KA, Estenne M, et al. Cyclosporine A drives a Th17-and Th2-mediated posttransplant obliterative airway disease. Am J Transplant (2013) 13(3):611-20. doi:10.1111/ajt.12067
51. Wang C, Yi T, Qin L, Maldonado RA, von Andrian UH, Kulkarni S, et al. Rapamycin-treated human endothelial cells preferentially activate allogeneic regulatory T cells. J Clin Invest (2013) 123(4):1677-93. doi:10.1172/JCI66204
52. Golshayan D, Jiang S, Tsang J, Garin MI, Mottet C, Lechler RI. In vitro-expanded donor alloantigen-specific CD4+CD25+ regulatory T cells promote experimental transplantation tolerance. Blood (2007) 109(2):827-35. doi:10.1182/blood-2006-05-025460
53. Sagoo P, Ali N, Garg G, Nestle FO, Lechler RI, Lombardi G. Human regulatory T cells with alloantigen specificity are more potent inhibitors of alloimmune skin graft damage than polyclonal regulatory T cells. Sci Transl Med (2011) 3(83):83ra42. doi:10.1126/scitranslmed.3002076
54. Tsang JY, Tanriver Y, Jiang S, Xue SA, Ratnasothy K, Chen D, et al. Conferring indirect allospecificity on CD4+CD25+ Tregs by TCR gene transfer favors transplantation tolerance in mice. J Clin Invest (2008) 118(11):3619-28. doi:10.1172/JCI33185
55. Tsang J, Jiang S, Tanriver Y, Leung E, Lombardi G, Lechler RI. In-vitro generation and characterisation of murine CD4+CD25+ regulatory T cells with indirect allospecificity. Int Immunopharmacol (2006) 6(13):1883-8. doi:10.1016/j.intimp.2006.07.032